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The Phylogenetic Position of a New Species of Plakobranchus From A peer-reviewed open-access journal ZooKeys 594: 73–98The (2016)phylogenetic position of a new species of Plakobranchus from West Papua... 73 doi: 10.3897/zookeys.594.5954 RESEARCH ARTICLE http://zookeys.pensoft.net Launched to accelerate biodiversity research The phylogenetic position of a new species of Plakobranchus from West Papua, Indonesia (Mollusca, Opisthobranchia, Sacoglossa) María Angélica Meyers-Muñoz1, Gerard van der Velde1,2, Sancia E.T. van der Meij2,3, Bart E.M.W. Stoffels1, Theo van Alen4, Yosephine Tuti5, Bert W. Hoeksema2 1 Radboud University Nijmegen, Institute for Water and Wetland Research, Department of Animal Ecology and Physiology, P.O. Box 9010, 6500 GL Nijmegen, The Netherlands2 Naturalis Biodiversity Center, Dar- winweg 2, 2333 CR Leiden, The Netherlands 3 Oxford University Museum of Natural History, Parks Road, Oxford OX1 3PW, United Kingdom 4 Radboud University Nijmegen, Institute for Water and Wetland Rese- arch, Department of Microbiology, P.O. Box 9010, 6500 GL Nijmegen, The Netherlands5 Research Centre for Oceanography (RCO), Indonesian Institute of Sciences (LIPI), Jl. Pasir Putih I, Ancol Timur, Jakarta 14430, Indonesia Corresponding author: Bert W. Hoeksema ([email protected]) Academic editor: N. Yonow | Received 29 October 2014 | Accepted 9 May 2016 | Published 30 May 2016 http://zoobank.org/570A4DC3-0CA8-4F7A-967F-3AED002FC3F4 Citation: Meyers-Muñoz MA, van der Velde G, van der Meij SET, Stoffels BEMW, van Alen T, Tuti Y, Hoeksema BW (2016) The phylogenetic position of a new species of Plakobranchus from West Papua, Indonesia (Mollusca, Opisthobranchia, Sacoglossa). ZooKeys 594: 73–98. doi: 10.3897/zookeys.594.5954 Abstract Plakobranchus papua Meyers-Muñoz & van der Velde, sp. n. from West Papua (Papua Barat province, Indonesia), is described based on its external morphology, colour pattern, internal anatomy, radula and reproductive system. In a molecular phylogenetic study specimens of this new species were compared with those of ten candidate taxa under the name Plakobranchus ocellatus van Hasselt, 1824. DNA analyses of COI mtDNA showed a clear distinction between P. papua sp. n. and “P. ocellatus”. Plakobranchus papua, sp. n. also differed from all taxa that have been synonymised withP. ocellatus. The genus is in dire need of taxonomic revision, preferably based on an integrative analysis involving morphology and DNA of all known Plakobranchus varieties. Keywords COI, phylogeny, Plakobranchus ocellatus, reproductive system, Sacoglossa, taxonomy Copyright María Angélica Meyers-Muñoz et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 74 María Angélica Meyers-Muñoz et al. / ZooKeys 594: 73–98 (2016) Introduction Sea slugs of the genus Plakobranchus van Hasselt, 1824 (Order Sacoglossa, Suborder Pla- kobranchacea) have an elongated body and dorsoventrally flattened, lateral parapodia, which are folded up on the dorsal surface (van Hasselt 1824; Jensen 1992). According to Jensen (1997a) this genus possesses a number of plesiomorphic characters such as an anterodorsal anus, a pharyngeal pouch, triangular, denticulate teeth, a long, curved penial stylet, and the absence of dorsal vessels. The genus also possesses a number of autapomor- phies: a broad and flat head, rhinophores located at the anterior corners, mediodorsal eyes on a small papilla, numerous longitudinal dorsal lamellae containing branches of the digestive gland, and a truncate tail; the hermaphrodite ampulla has apparently been lost. These animals can be found in shallow sandy habitats, crawling over it or half- buried (Gosliner et al. 2008; Mehrotra et al. 2015), or on coral rubble and in rock pools (Yonow 2008) where they consume green macroalgae (Jensen 1993). Plakobranchus ocellatus van Hasselt, 1824, feeds on a wide variety of marine green algae (Chlorophyta), including at least five species of Ulvophyceae (Wägele et al. 2011). Many studies on Plakobranchus deal with their kleptoplasty, the ability to retain functional chloroplasts from their green algae in their digestive gland cells (Clark et al. 1990; Jensen 1996, 1997a). Species of this genus as well as other sacoglossans belong to the few known animal species with the ability of photosynthesis (Trench 1969; Hirose 2005; Bass 2006; Händeler et al. 2009; Maeda et al. 2010; Wägele et al. 2011; Christa et al. 2013; Yamamoto et al. 2013). Plakobranchus species are simultaneous hermaphrodites, which possess a penial sty- let used in hypodermic insemination. Penial stylets and hypodermic insemination are commonly found within the Sacoglossa (Schmitt et al. 2007; Smolensky et al. 2009). Jensen (1992) also observed extensively branched prostate and albumen glands and a pair of secondary copulatory bursae in Plakobranchus, which are unique for the genus. During the last decades only Plakobranchus ocellatus has been considered a valid spe- cies within the genus (Jensen 1992). This species was described from shallow waters in the Sunda Strait near Anyer, northwest Java, Indonesia. van Hasselt (1824) gave this name because of the blue- and yellow-centred ocellated spots covering the dorsal side and flanks of the body (Figure 1). The original description is based on the species’ phenotype and some characteristics of the parapodial lamellae, heart and reproductive system as shown in the original illustrations supplied by van Hasselt (1824). The namePlakobranchus has occasionally been misspelled as Placobranchus, which started when the original description was translated from Dutch to French in 1824 (Bergh 1887; Jensen 1997a, 1997c). Jensen (1992) studied the anatomy of several Plakobranchus specimens from vari- ous Indo-West Pacific locations (Red Sea, Thailand, Guam) and synonymised the previously described species. The descriptions were mainly based on external anato- my, colour pattern and geographic distribution (Yonow 1990, 2008; Debelius 1996; Jensen 1997a; Marshall and Willan 1999; Gosliner et al. 2008) and hardly included descriptions of the internal anatomy as presented by van Hasselt (1824) and Jensen (1992). Plakobranchus ocellatus is now considered the only known valid species of the The phylogenetic position of a new species of Plakobranchus from West Papua... 75 Figure 1. a–c Plakobranchus ocellatus, drawings by van Hasselt (1824): a dorsal view with parapodia folded up on the dorsal body surface b dorsal view with open parapodia, showing longitudinal lamellae c internal anatomy d–f P. ianthobaptus, drawings by Gould (1852): d dorsal view with parapodia folded up on the dorsal body surface e ventral view f dorsal view with open parapodia, showing longitudinal lamel- lae g–j two Plakobranchus species illustrated by Pease (1871) g–h P. gracilis: g ventral view h dorsal view i–j P. variegatus: i ventral view j dorsal view k–l drawings of P. chlorophacus by Bergh (1873): k dorsal view with parapodia folded up on the dorsal body surface l ventral view with ocellated spots m–n drawings of P. ocellatus by Marcus (1982): m dorsal view with parapodia folded up on the dorsal body surface n dorsal view with open parapodia, showing the longitudinal lamellae (en = pericardium; re = renal prominence). 76 María Angélica Meyers-Muñoz et al. / ZooKeys 594: 73–98 (2016) genus, with ten synonyms and a wide Indo-Pacific distribution (Jensen 2007). This may have been premature (Jensen 1992, 1997a, 1997c), because Gosliner et al. (2008) distinguished two undescribed Plakobranchus species in addition to P. ocellatus. Sub- sequently, Krug et al. (2013), who used the mitochondrial barcoding gene COI and the nuclear histone 3 gene, found ten distinct phylogenetic lineages in Plakobranchus. This suggests that the taxonomy ofPlakobranchus still deserves further study. In the present study a new Plakobranchus species from West Papua, Indonesia, is described and a phylogenetic reconstruction based on the mitochondrial barcoding COI gene is included to show its position within the genus Plakobranchus. Material and methods Twenty specimens were collected by Gerard van der Velde in Indonesia during the 2007 Raja Ampat Expedition (Figure 2; Hoeksema and van der Meij 2008). The speci- mens were observed alive, photographed, and subsequently preserved in 96% ethanol. Material analysed in this study was deposited in the mollusc collection of Natura- lis Biodiversity Center, Leiden, The Netherlands, and catalogued as RMNH.MOL. One specimen of P. ocellatus (RMNH.MOL.336426), collected in the Philippines, 4 November 1999 (Sta. CEB.01, Cebu Strait, E side of Olango Island 10°15'54"N 124°04'17"E, coll. BWH) was used for comparison of external characters with the new species in absence of the holotype of P. ocellatus (Figures 7b–d). The original draw- ings of van Hasselt (1824) are available in scientific archives of Naturalis Biodiversity Center and reprinted here (Figures 1a–c). To study the radula, the buccal masses of two specimens were dissected and im- mersed in 10% NaOH until the tissue surrounding the radulae was dissolved. The radulae were rinsed in distilled water and transferred to 70% ethanol. They were sub- sequently examined by means of a light microscope, photographed, mounted on stubs, and gold-sputter-coated for scanning electron microscopy (SEM). Eight specimens were dissected for anatomical studies. One specimen (Table 1) was dehydrated in a graded ethanol series, embedded in
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